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The gastric cavity of corals as bioreactor fo ecosystem-scale microbial processes

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Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching
Publication . Rodrigues Frade, Pedro; Bongaerts, Pim; Englebert, Norbert; Rogers, Alice; Gonzalez-Rivero, Manuel; Hoegh-Guldberg, Ove
Our rapidly warming climate is threatening coral reefs as thermal anomalies trigger mass coral bleaching events. Deep (or "mesophotic") coral reefs are hypothesised to act as major ecological refuges from mass bleaching, but empirical assessments are limited. We evaluated the potential of mesophotic reefs within the Great Barrier Reef (GBR) and adjacent Coral Sea to act as thermal refuges by characterising long-term temperature conditions and assessing impacts during the 2016 mass bleaching event. We found that summer upwelling initially provided thermal relief at upper mesophotic depths (40 m), but then subsided resulting in anomalously warm temperatures even at depth. Bleaching impacts on the deep reefs were severe (40% bleached and 6% dead colonies at 40 m) but significantly lower than at shallower depths (60-69% bleached and 8-12% dead at 5-25 m). While we confirm that deep reefs can offer refuge from thermal stress, we highlight important caveats in terms of the transient nature of the protection and their limited ability to provide broad ecological refuge.
Establishing microbial baselines to identify indicators of coral reef health
Publication . Glasl, Bettina; Bourne, David G.; Rodrigues Frade, Pedro; Webster, Nicole S.
Microorganisms make a significant contribution to reef ecosystem health and resilience via their critical role in mediating nutrient transformations, their interactions with macro-organisms and their provision of chemical cues that underpin the recruitment of diverse reef taxa. However, environmental changes often cause compositional and functional shifts in microbial communities that can have flow-on consequences for microbial-mediated processes. These microbial alterations may impact the health of specific host organisms and can have repercussions for the functioning of entire coral ecosystems. Assessing changes in reef microbial communities should therefore provide an early indicator of ecosystem impacts and would underpin the development of diagnostic tools that could help forecast shifts in coral reef health under different environmental states. Monitoring, management and active restoration efforts have recently intensified and diversified in response to global declines in coral reef health. Here we propose that regular monitoring of coral reef microorganisms could provide a rapid and sensitive platform for identifying declining ecosystem health that can complement existing management frameworks. By summarising the most common threats to coral reefs, with a particular focus on the Great Barrier Reef, and elaborating on the role of microbes in coral reef health and ecosystem stability, we highlight the diagnostic applicability of microbes in reef management programs. Fundamental to this objective is the establishment of microbial baselines for Australia's coral reefs.
eDNA metabarcoding for diet analyses of green sea turtles (Chelonia mydas)
Publication . Díaz-Abad, Lucía; Bacco-Mannina, Natassia; Madeira, Fernando Miguel; Neiva, J.; Aires, Tania; Serrao, Ester; Regalla, Aissa; Patrício, Ana R.; Rodrigues Frade, Pedro
Understanding sea turtle diets can help conservation planning, but their trophic ecology is complex due to life history characteristics such as ontogenetic shifts and large foraging ranges. Studying sea turtle diet is challenging, particularly where ecological foraging observations are not possible. Here, we test a new minimally invasive method for the identifcation of diet items in sea turtles. We fngerprinted diet content using DNA from esophageal and cloacal swab samples by metabarcoding the 18S rRNA gene. This approach was tested on samples collected from green turtles (Chelonia mydas) from a juvenile foraging aggregation in the Bijagós archipelago in Guinea-Bissau. Esophagus samples (n=6) exhibited a higher dietary richness (11±5 amplicon sequence variants (ASVs) per sample; average±SD) than cloacal ones (n=5; 8±2 ASVs). Overall, the diet was dominated by red macroalgae (Rhodophyta; 48.2±16.3% of all ASVs), with the main food item in the esophagus and cloaca being a red alga belonging to the Rhodymeniophycidae subclass (35.1±27.2%), followed by diatoms (Bacillariophyceae; 7.5±7.3%), which were presumably consumed incidentally. Seagrass and some invertebrates were also present. Feeding on red algae was corroborated by feld observations and barcoding of food items available in the benthic habitat, validating the approach for identifying diet content. We conclude that identifcation of food items using metabarcoding of esophageal swabs is useful for a better understanding of the relationships between the feeding behavior of sea turtles and their environment.
Red, gold and green: microbial contribution of Rhodophyta and other Algae to Green Turtle (Chelonia mydas) Gut Microbiome
Publication . Díaz-Abad, Lucía; Bacco-Mannina, Natassia; Miguel Madeira, Fernando; Serrao, Ester; Regalla, Aissa; Patrício, Ana R.; Rodrigues Frade, Pedro
The fitness of the endangered green sea turtle (Chelonia mydas) may be strongly affected by its gut microbiome, as microbes play important roles in host nutrition and health. This study aimed at establishing environmental microbial baselines that can be used to assess turtle health under altered future conditions. We characterized the microbiome associated with the gastrointestinal tract of green turtles from Guinea Bissau in different life stages and associated with their food items, using 16S rRNA metabarcoding. We found that the most abundant (% relative abundance) bacterial phyla across the gastrointestinal sections were Proteobacteria (68.1 ± 13.9% “amplicon sequence variants”, ASVs), Bacteroidetes (15.1 ± 10.1%) and Firmicutes (14.7 ± 21.7%). Additionally, we found the presence of two red algae bacterial indicator ASVs (the Alphaproteobacteria Brucella pinnipedialis with 75 ± 0% and a Gammaproteobacteria identified as methanotrophic endosymbiont of Bathymodiolus, with <1%) in cloacal compartments, along with six bacterial ASVs shared only between cloacal and local environmental red algae samples. We corroborate previous results demonstrating that green turtles fed on red algae (but, to a lower extent, also seagrass and brown algae), thus, acquiring microbial components that potentially aid them digest these food items. This study is a foundation for better understanding the microbial composition of sea turtle digestive tracts.
Microbial surface biofilm responds to the growth-reproduction-senescence cycle of the dominant coral reef macroalgae Sargassum spp.
Publication . Glasl, Bettina; Haskell, Jasmine B.; Aires, Tania; Serrao, Ester; Bourne, David G.; Webster, Nicole S.; Frade, Pedro Rodrigues
Macroalgae play an intricate role in microbial-mediated coral reef degradation processes due to the release of dissolved nutrients. However, temporal variabilities of macroalgal surface biofilms and their implication on the wider reef system remain poorly characterized. Here, we study the microbial biofilm of the dominant reef macroalgae Sargassum over a period of one year at an inshore Great Barrier Reef site (Magnetic Island, Australia). Monthly sampling of the Sargassum biofilm links the temporal taxonomic and putative functional metabolic microbiome changes, examined using 16S rRNA gene amplicon and metagenomic sequencing, to the pronounced growth-reproduction-senescence cycle of the host. Overall, the macroalgal biofilm was dominated by the heterotrophic phyla Firmicutes (35% ± 5.9% SD) and Bacteroidetes (12% ± 0.6% SD); their relative abundance ratio shifted significantly along the annual growth-reproduction-senescence cycle of Sargassum. For example, Firmicutes were 1.7 to 3.9 times more abundant during host growth and reproduction cycles than Bacteroidetes. Both phyla varied in their carbohydrate degradation capabilities; hence, temporal fluctuations in the carbohydrate availability are potentially linked to the observed shift. Dominant heterotrophic macroalgal biofilm members, such as Firmicutes and Bacteroidetes, are implicated in exacerbating or ameliorating the release of dissolved nutrients into the ambient environment, though their contribution to microbial-mediated reef degradation processes remains to be determined.

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Funding agency

Fundação para a Ciência e a Tecnologia

Funding programme

OE

Funding Award Number

SFRH/BPD/110285/2015

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